The Primate Peripheral Auditory System and the Evolution of Primate Hearing

Early comparative studies of mammalian/primate auditory anatomy were carried out in the nineteenth century (Hyrtl 1845; Doran 1879) and early twentieth century (van Kampen 1905; van der Klaauw 1931). During the decades since 1960, work by several researchers has moved from pure anatomical descriptions to augmenting the understanding of the functions of mammalian/primate auditory structures. The functional anatomy of the mammalian ear was promoted by Henson (1961, 1974), while Masterton et al. (1969) focused on the evolution of high-frequency hearing among mammals, including primates. Furthermore, Fleischer (1973, 1978) established a basis for future comparative studies in morphology and evolution of the middle and inner ear structures of a wide range of mammalian taxa. Cartmill (1975) and MacPhee (1979, 1981) were early pioneers in the study of the primate auditory region.

Previous reviews have described the diversity among mammalian ears and hearing. Differences in the contribution of each of the temporal bone elements to the construction of the ear region in different mammalian orders were presented in compilations by Novacek (1977, 1993). Research on mammalian hearing and the peripheral auditory system is firmly grounded in the work of Rosowski (1992, 2013). The relationship between the morphological variation of the mammalian ear and hearing characteristics was also studied by Hemilä et al. (1995) and by Nummela (1995). Vertebrate auditory physiology, evolution, and development are presented widely by Manley et al. (2004) and Manley (2014). A comparative view on hearing in the animal kingdom can be found in the review by Köppl et al. (2014). Experimental work on mammalian hearing and on the role of high-frequency hearing in sound localization combined morphological and experimental data (R. S. Heffner and H. E. Heffner 1992a; H. E. Heffner and R. S. Heffner 2014) that expanded the understanding of the significance of the auditory sense in an organism’s behavioral ecology.

Primate auditory morphology and its evolution since the Paleocene epoch received detailed attention through the research efforts of Coleman and Ross (2004) and Coleman and Boyer (2012). The primate cochlear labyrinth and its relationship to hearing abilities were studied by Kirk and Gosselin-Ildari (2009) and Armstrong et al. (2011). Auditory capacities in fossil hominins were estimated from the anatomy of the outer and middle ears by Martínez et al. (2004) and Quam et al. (2015). For vertebrates in general, the evolution of the ear and hearing is treated by Clack et al. (2016), and vertebrate sound production and acoustic communication is discussed by Suthers et al. (2016).

The two primary methods for measuring the hearing sensitivity of an animal are behavioral testing and auditory brainstem recordings to obtain audiograms, and comparisons of these methods are a matter of discussion (Ramsier and Dominy 2010; Ramsier and Rauschecker, Chap. 3). A comprehensive selection of vertebrate audiograms can be found in Fay (1988). Here, a selection of behavioral audiograms for primates will be presented. A human behavioral audiogram (Fig. 2.2) shows the general characteristics that are often of interest in an animal’s hearing. These include the overall hearing range, the low- and high-frequency limits (the lowest and highest frequency heard at 60 dB SPL), the best sensitivity (in dB), and the best frequency (the frequency heard at the best sensitivity). Behavioral audiograms are shown separately for a few strepsirrhines, platyrrhines, and catarrhines (Figs. 2.3, 2.4 and 2.5). The behaviorally measured auditory parameters are often used for finding possible correlations between hearing sensitivity and auditory morphology in primates and determining how different structures affect the hearing characteristics of a species; the outer, middle, and inner ears all are known to contribute to this (Ruggero and Temchin 2002; Vater et al. 2004). This is discussed more in Sects. 2.2, 2.3.3, and 2.4.

Fig. 2.2

Average human audiograms from three separate studies. The thick gray line indicates the audiograms measured with the conditions described by Jackson et al. (1999). Standard audiograms from Sivian and White (1933) (dashed line) and from Davis (1960) (thin line) are indicated for comparison. Common audiometric parameters used for describing hearing sensitivity are indicated, with the hearing range customarily set between high- and low-frequency limits at 60 dB SPL. (Reprinted with permission from R. S. Heffner 2004)

Fig. 2.3

Average audiograms for strepsirrhines (formerly known as prosimians): ring-tailed lemur (Lemur catta), lesser bushbaby (Galago senegalensis), potto (Perodicticus potto), and Sunda slow loris (Nycticebus coucang). The audiogram of the tree shrew (Tupaia glis; Scandentia), a species closely related to primates, is also shown. The thick gray line is the human audiogram. (Modified and reprinted with permission from R. S. Heffner 2004)

Hearing is a particularly important sensory modality since it allows perception of phenomena that might be out of sight. To take advantage of any potential information carried by sound (e.g., vocalizations), an organism has to perform at least one of three basic auditory tasks: sound detection, sound localization, and sound identification (R. S. Heffner 2004; Yost et al. 2008). Although animals are capable of performing these practically simultaneously, sound detection is still the most basic of these tasks since it underlies the other two. Of the various ways to measure and describe hearing sensitivity, a behavioral audiogram provides insights into what an animal actually hears (see Ramsier and Rauschecker, Chap. 3), and the behavior of an entire organism is generally considered the target for selective pressure (R. S. Heffner 2004).

Primates make use of different sound frequencies (Ramsier and Rauschecker, Chap. 3), they live in different habitats with different acoustics (Brown and Waser, Chap. 4), and they vary in body size (Smith and Jungers 1997; Mattila and Bokma 2008). In general, primate hearing sensitivity follows phylogenetic patterns. Coleman (2009) provided a comprehensive overview of all published nonhuman primate behavioral audiograms, both speaker derived and headphone derived. The best high-frequency hearing among the extant primates tested has been found in strepsirrhines (lemurs and lorises) and tarsiers, whereas low-frequency sensitivity is generally better in haplorhines (monkeys and apes) (R. S. Heffner 2004; Ramsier et al. 2012a). Within haplorhines, the catarrhines are generally more sensitive to lower frequencies than are the platyrrhines, and high-frequency sensitivity is reduced in apes compared with monkeys. Furthermore, monkeys and apes (except humans) often show two peaks of maximum sensitivity, whereas lemurs and lorises, as well as humans, generally have only a single peak in sensitivity in their audiograms (Coleman 2009; Ramsier and Rauschecker, Chap. 3).

2.2 Outer Ear and Interaural Distance

Mammals are the only vertebrates with a distinct outer ear that consists of a pinna and the ear canal (external auditory meatus). Both of these structures show large morphological variation among mammals. The pinna varies in its height and width, location on the head, and size in relation to the head size. The outer ear canal varies in its overall geometry, length, and cross-sectional area. A larger pinna can collect a larger amount of sound energy and is also more suitable for the long wavelengths of low frequencies (R. S. Heffner et al. 1982; Ahlborn 2004). The level of amplification of the incoming sound performed by the outer ear depends directly on the size of the pinna and, especially, on the length of the ear canal (Dallos 1973; Zwislocki 1975).

All primates possess cartilaginous pinnae, which show considerable diversity in prominence, morphology, and mobility (Fig. 2.6). There is also variation in the placement of the pinnae on the head, how much the pinnae protrude above the head, and whether they are covered by fur or not (Packer and Sarmiento 1984). Relative to head size, the pinna is larger in strepsirrhines than in haplorhines, with the largest pinnae found in aye-ayes (Daubentonia madagascariensis) (Coleman and Ross 2004) and the smallest ones in orangutans (Pongo pygmaeus) (Schultz 1973). In strepsirrhines, the auricular musculature is better developed, and the pinnae are generally more mobile and protrude more above the head than in haplorhines (Coleman and Ross 2004; Fleagle 2013). The large morphological variation of the primate pinna (Fig. 2.6) generally follows phylogeny but also has ecological patterns. Strepsirrhines and tarsiers, both of which include many nocturnal species, have relatively tall and narrow pinnae, whereas platyrrhines and catarrhines, which are mostly diurnal species, have shorter, wider, and more symmetrical pinnae. While no functional significance has been attributed to these shape differences, they may still be useful in primate systematics (Coleman and Ross 2004; Coleman and Colbert 2010).

The length of the bony portion of the outer ear canal was measured on dry skulls by Masali et al. (1992) for small samples of humans, chimpanzee (Pan troglodytes), gorilla (Gorilla gorilla), and orangutan. The cartilaginous portion of the ear canal was estimated to form one-third of the total length in humans, and the total ear canal length was calculated as one-and-a-half times the length of the bony portion for all the ape species. The fundamental resonance frequency of the outer ear canal (the frequency of maximum dB gain) was estimated from its length and was around 3.0 kHz in humans, while the apes ranged between approximately 1.5–2.0 kHz.

The correspondence between the fundamental resonance frequency of the external auditory meatus and the frequency of best hearing sensitivity can be examined. The best frequency for humans is around 3 kHz (Fig. 2.2) and the fundamental resonance frequency is 3.1 kHz. For the chimpanzee, the best frequency is around 2 kHz (Elder 1934; Masterton et al. 1969) and the fundamental resonance frequency is 2.15 kHz (Masali et al. 1992). A close association between the best-heard frequencies and the central portion of the frequency range of human language is well-known (Shaw 1974), and the fundamental resonance frequency of the ear canal also corresponds to the modal pitch of long-distance calls in the other ape species. The lower frequencies of best sensitivity in apes (compared with humans) might be advantageous in a forested environment where low frequencies propagate better (Masali et al. 1992; Brown and Waser, Chap. 4).

Sound localization is of vital importance for the survival of an animal and has most likely been under selective pressure during the evolution of mammals (H. E. Heffner and R. S. Heffner 2016). In addition to head movements, mammals can use their movable pinnae when locating a sound source and directing the eyes to it, thus enabling the animal to add another sense to the sound localization task (Masterton et al. 1969; R. S. Heffner and H. E Heffner 1992a; also see Sect. 2.6). Large animals with a large interaural distance can use the interaural time difference for sound localization, but for small animals with a small head, including many primate species, the interaural intensity difference is especially useful at higher frequencies.

Figure 2.7 shows how the high-frequency hearing limit is related to the maximum functional interaural distance (interaural distance divided by sound velocity, in microseconds) in over sixty different mammals. The sixteen primate species included do not deviate from the general mammalian pattern in this respect (Masterton et al. 1969; R. S. Heffner and H. E Heffner 1992a). Better high-frequency hearing is correlated with smaller interaural distance. With some exceptions among other vertebrates, only mammals hear frequencies over 10 kHz (Fay 1988). Indeed, the ability to hear high frequencies gives the advantage of using spectral cues if an animal has a pinna to produce these cues for sound localization (R. S. Heffner 2004).

Fig. 2.7

Relationship between maximum functional interaural distance (the time for a sound in air or water to travel from one ear canal to the other) and the high-frequency hearing limit at 60 dB SPL for over sixty mammals. Filled circles: primates, with species referenced earlier and the brown lemur (Eulemur fulvus), three guenons (Cercopithecus sp.), and the yellow baboon; open circles: selection of other mammals; open triangles: subterranean mammals (not included in the statistical analysis). (Reprinted with permission from R. S. Heffner 2004)

Coleman and Colbert (2010) studied the relationship between the measured interaural distance and frequency sensitivity (sound pressure level at 32 kHz taken from an animal’s audiogram) in a sample of eleven taxonomically diverse primate species. Even with this smaller sample size, they found a similarly strong correlation as found by R. S. Heffner (2004). The few departures were the yellow baboon (Papio cynocephalus), which showed relatively good high-frequency hearing, and the Japanese macaque (Macaca fuscata) and the Sunda slow loris (Nycticebus coucang), which both had somewhat poor high-frequency sensitivity relative to interaural distance. In this particular study, these findings may simply be due to methodological differences. Coleman and Colbert (2010) suggested that in the case of baboons, some other ecological factors related to communication could explain the exceptionally good sensitivity to high frequencies. For the macaque and the loris, other anatomical or ecological factors may be impairing the high-frequency sensitivity that is predicted by the interaural distance.

2.3 Middle Ear

2.3.1 Temporal Bone

The anatomical divisions of the primate temporal bone (squamous, petrous, and tympanic) have large contacts with each other, and the temporal bone articulates with other cranial bones as well (Novacek 1977, 1993). As a result, the ear is not acoustically isolated from the skull, and sound waves can travel through the skull. Primates are the only mammals with an auditory bulla formed solely by the petrous part (petrosal) of the temporal bone (Cartmill et al. 1981; MacPhee 1981). The auditory bulla surrounds the middle ear cavity (Table 2.1; Fig. 2.8). In strepsirrhines, the petrosal is expanded into a balloon-like protrusion and forms a comparatively inflated auditory bulla. Lemurs have a single-chambered middle ear cavity, whereas lorises exhibit a two-chambered middle ear cavity with additional air-filled space in the form of an anterior accessory cavity, but there is no diverticulum (Cartmill 1972, 1975). In tarsiers, which are small nocturnal haplorhines, the auditory bulla is fairly large and located almost in the center of the cranial base, close to the foramen magnum. As a result, the left and right bullae are near one another. As for other haplorhines, in many New World monkeys the petrosal is similar to that in strepsirrhines, whereas in Old World monkeys and apes (including humans), the petrosal has a rough texture on its ventral surface and does not form a balloon-like structure. Haplorhines have a two-chambered middle ear cavity with a posterior accessory cavity with air-filled spaces off of the epitympanic recess and a diverticulum off of the Eustachian tube (Packer and Sarmiento 1984; MacPhee and Cartmill 1986).

Table 2.1

Ear characteristics among different primate groups. For further information, see Sect. 2.3.1

Strepsirrhines

Haplorhines

Lemuroids

Lorisoids

Tarsiers

New World monkeys (platyrrhines)

Old World monkeys and apes (catarrhines)

Petrosal

Forms the auditory bulla in strepsirrhines and haplorhines

Auditory bulla

Balloon-like and inflated

Enlarged and situated close to the foramen magnum

Balloon-like and inflated (in most species)

Not balloon-like, rough texture ventrally

Middle ear cavity

Single chambered

Two-chambered: anterior accessory cavity with air-filled spaces, but no diverticulum

Two chambered: posterior accessory cavity with air-filled spaces off the epitympanic recess and a diverticulum off the Eustachian tube

Tympanic

Forms complete bony ring or bony tube in all primates

Bony ring/bony tube

Bony ring unfused to the bulla (free floating)

Bony ring fused to the bulla

Bony tube fused to the bulla

Bony ring fused to the bulla

Bony tube fused to the bulla

Outer ear canal

Almost entirely cartilaginous, no bony tube

Elongated tympanic forms the bony part

Almost entirely cartilaginous, no bony tube

Elongated tympanic forms the bony part

Fig. 2.8

Variations in the temporal bone anatomy of primates: ventral view (above) and cross-sectional view of the ear region (below). The petrous, the tympanic, and the squamosal portions vary considerably across different taxa (also see Table 2.1). In lemurs, the tympanic (ectotympanic) bone supporting the eardrum is ring-shaped, suspended within the tympanic cavity, and surrounded by the petrous portion. In lorises, the tympanic is connected to the wall of the bulla and the bulla cavity is divided. The tympanic bone is an elongated bony tube on the lateral side of the skull in tarsiers and in Old World monkeys and apes (including humans). In New World monkeys the tympanic forms a tympanic ring that is fused to the auditory bulla laterally. (Modified and reprinted with permission from Fleagle 2013)

In primates, as in moles, many rodents, and elephants, the insertion site for the tympanic membrane takes the form of a complete bony ring (Table 2.1; Fig. 2.9), whereas in some other mammals (e.g., artiodactyls and perissodactyls) the insertion is U-shaped (van der Klaauw 1931; Fleischer 1973). Within strepsirrhines, the tympanic bone consists solely of a bony ring. In lemurs, this ring is unfused (free floating) within the middle ear cavity (Fig. 2.8), but it is still surrounded by the relatively large, single-chambered auditory bulla, whereas in lorises, the tympanic ring is fused to the wall of the bulla (Cartmill 1975). Within haplorhines, New World monkeys resemble lorises in having a laterally fused tympanic ring. In catarrhines, as well as in tarsiers, the tympanic bone is likewise fused to the bulla wall, but instead of forming a single ring, the tympanic forms a bony tube. This elongated bony tube extends laterally toward the external ear opening at the side of the skull and forms the outer ear canal. Strepsirrhines and platyrrhines do not possess this bony tube but have only a tympanic ring, and their external auditory meatus is almost entirely cartilaginous (Table 2.1).

Fig. 2.9

Middle ear ossicles from the left ear of three primate species as viewed from inside the middle ear cavity. Left: Greater bushbaby (strepsirrhine, lorisoid); middle: macaque (haplorhine, Old World monkey); right: chimpanzee (haplorhine, ape). The contours of the tympanic membrane are shown for each as well as the area of the stapes footplate (FP). Tympanic membrane diameters measured perpendicular to the manubrium of the malleus are 5.0 mm, 7.5 mm, and 10.2 mm, respectively. (Reprinted with permission from Fleischer 1973)

2.3.2 Middle Ear Structure and Function

The primate middle ear has the general mammalian anatomy with three middle ear ossicles (malleus, incus, and stapes) forming an ossicular chain in the cavity between the tympanic membrane laterally and the oval window of the cochlea medially (Figs. 2.1 and 2.9). In primates, as in most mammals, the malleus is attached to the tympanic membrane at its lower, slender part called the manubrium. The anterior process of the malleus (also called the gonial or the processus gracilis) makes contact with the tympanic ring anteriorly. The looseness/stiffness of this contact varies among different mammals. In turn, the malleus head and the incus body articulate with one another (incudomalleolar joint). The incus has a small lenticular process at the tip of its long process, and this lenticular process articulates with the stapes head (incudostapedial joint). The medial end of the stapes (the footplate) is attached to the oval window of the cochlea.

In sound transmission, from the lower acoustic impedance of air in the ear canal to the much higher acoustic impedance of the fluid-filled inner ear (Rosowski 1994; Hemilä et al. 1995), the middle ear acts as an acoustic impedance-matching device that compensates for the loss in energy associated with this change in medium. The mass and stiffness of the ossicles are the main factors limiting transmission at higher frequencies; the middle ear cavity volume and the tightness of the connections between the malleus and tympanic membrane and at the joints between the ossicles are the main limiting factors at lower frequencies. Smaller middle ears with smaller tympanic membranes, lighter ossicles, and tighter connections between them are better at transmitting higher frequencies while larger middle ears with larger tympanic membranes, heavier ossicles, and looser connections between them are better suited for transmitting lower frequencies (Møller 1974; Rosowski and Relkin 2001).

This impedance matching in land mammals is accomplished by the area ratio, which is the ratio between the tympanic membrane area and the oval window area, and by the lever ratio, which is the ratio between the malleus lever arm length and the incus lever arm length (Rosowski 1994; Nummela et al. 2007). The impedance transformer ratio is the product of these two ratios: [(area ratio) × (lever ratio)2]. Although the middle ear is often seen as a pressure-enhancing mechanism between the surrounding air and the inner ear fluid, it is evident that the earliest land vertebrates did not have such an impedance-matching mechanism in their ears (Manley and Sienknecht 2013). Additionally, the middle ear transmission mechanism is not solely responsible for the hearing sensitivity of mammals. Rather, the outer, middle, and inner ears together are important for determining the overall shape of an animal’s audiogram (Ruggero and Temchin 2002; Hemilä et al. 2010).

In an ideal case, the impedance-matching system of the middle ear would offset the loss of sound energy when changing from the air-filled environment to the fluid-filled cochlea. Nevertheless, the theoretical pressure gain based on the ideal impedance transformer ratio of the middle ear does not correspond to empirical results of middle ear pressure gain measured in experimental settings (Rosowski and Relkin 2001).

2.3.3 Middle Ear Morphology and Hearing Sensitivity

Detailed anatomical descriptions on the comparative morphology of mammalian ossicles, including twenty-five primate species from all major taxonomic groups, can be found in Doran (1879), who separated primate ossicles into four groups (as did Hyrtl 1845): (1) humans, (2) apes, (3) Old World monkeys, and (4) New World monkeys and strepsirrhines. Likewise, Masali et al. (1992) identified two grouping for primate ossicles: (1) the Old World primate type, and (2) the New World primate and strepsirrhine type. This grouping mirrors the temporal bone similarities between these two groups (Sect. 2.3.1; Table 2.1).

Based on a wide, systematic survey of the morphology of the mammalian peripheral auditory region, including twenty-five primate species, Fleischer (1973, 1978) studied the evolutionary history of the mammalian middle ear and, particularly, of the malleus-incus complex. Detailed morphological descriptions and quantitative models for ossicular chain function were also presented. Fleischer identified four middle ear types across mammals: the ancestral ear, the microtype ear, the transitional ear (also called the intermediate ear), and the freely mobile ear. He suggested that an ancestral middle ear type had given rise to the other three types. A central role in grouping the middle ear types was given to the anterior process of the malleus. This structure varies in size and in strength of attachment to the tympanic ring. Hence, the different ear types deviate from each other by how loose or tight the connections are between different parts.

In the ancestral ear and the microtype ear, the malleus is tightly attached to the tympanic ring with its long anterior process, and the connection between the malleus and the incus is firm (although not ossified) with the joint surfaces being tightly interlocked. These kinds of ears are best suited for transmitting high-frequency sounds and are found in small mammals, such as bats and rodents. The two other types, the transitional ear and the freely mobile ear, are found among primates (Fig. 2.9). In the transitional middle ear (e.g., greater bushbaby, Otolemur crassicaudatus, for which the old name Galago crassicaudatus was used by Fleischer 1973), the anterior process of the malleus has only a loose contact with the tympanic ring, and the joint between the malleus and incus is not as tight as in the microtype ear. In the freely mobile middle ear (e.g., macaque, Macaca sp., and chimpanzee), the anterior process of the malleus has been reduced and is loose from the tympanic ring; the joint between the malleus and incus is also loose with more mobility between the ossicles than in the transitional ear or the microtype ear. The head of the malleus is larger in the freely mobile ear, and the incus is relatively larger as compared to the malleus than in the other two types (Fig. 2.9).

Based on the sizes of the tympanic membrane and stapes footplate in over fifty mammalian species, including three primates (bushbaby, macaque, and chimpanzee), Fleischer (1973) concluded that the middle ear size is not totally dependent on body size (mass). Nevertheless, strong correlations between both tympanic membrane and stapes footplate area with body mass were found across mammals (Hunt and Korth 1980; Rosowski and Graybeal 1991). The size variation in both the tympanic membrane and the oval window is clearly negatively allometric to body mass in mammals in general, including primates (Rosowski 1994). In addition, a strong correlation was found between ossicular mass and body mass across both placental and marsupial taxa (Nummela 1995; Nummela and Sánchez-Villagra 2006). In contrast, the relationships between different middle ear structures themselves (i.e., tympanic membrane and oval window areas; malleus and incus lever arms and masses) are highly isometric among mammals, including primates (Rosowski 1992; Hemilä et al. 1995). Within primates, Coleman et al. (2010) showed that the areas of the tympanic membrane and stapes footplate are strongly correlated with body mass across a large number of strepsirrhine and catarrhine taxa. They also found a strong correlation between the tympanic membrane and the stapes footplate areas for these same species.

Rosowski (1992) divided twenty mammals, including three primate species, into three groups according to their middle ear type (microtype, transitional, or freely mobile type) sensu Fleischer (1973, 1978) and established their low- and high-frequency hearing limits (at 60 dB SPL) and their best frequency on the basis of the behavioral audiogram for each species. These audiometric parameters were then compared with anatomical measurements to establish correlations between ear structure and function. Each mammalian group had a distinct hearing range with only limited overlap. The strongest correlations were found between the best frequency and the tympanic membrane area and for the low- and high-frequency limits with the footplate area. Thus, increases in body size and corresponding increases in the sizes of the tympanic membrane and the stapes footplate lead to a lowering of the best frequency and the low- and high-frequency limits.

It is evident that the middle ear structures and auditory capacities of extant mammals vary widely, and attempts to correlate these two can reveal significant relationships, which in turn can be used to predict the auditory capacities of fossil mammals for which only structural data are available (Nummela et al. 2004; Quam et al. 2013). Plassmann and Brändle (1992) developed a general model to explain auditory function from structural measurements that was applicable to a wide diversity of mammalian species with different ear dimensions, including tympanic membrane radius, the middle ear volume radius, the cross-sectional area and length of the external auditory meatus, and the frequency of best sensitivity. The tympanic membrane area and the middle ear volume have identical resonance frequencies in each species studied, and it is possible to predict the tympanic membrane size on the basis of the frequency range of best sensitivity and vice versa. Similarly, Hemilä et al. (1995) have shown that the behavioral high-frequency limit is inversely related to the cube root of the combined mass of the malleus and incus across twenty-eight mammalian species, including nine primates. These models can potentially be applied to fossil specimens to predict aspects of their unknown audiograms (see Quam, Martínez, Rosa, and Arsuaga, Chap. 8).

The impedance transformer ratio was studied for thirty-three primate taxa by Coleman and Ross (2004). The area ratio was found not to differ significantly between haplorhines and strepsirrhines, reflecting the largely isometric relationship between these two variables (Sect. 2.3.2). However, clear differences exist in the lever ratio, with strepsirrhines showing a higher lever ratio than haplorhines. These differences are independent of variation in body size but seem to reflect differences in malleus lever arm length, suggesting that differences in the impedance transformer ratio among primates are primarily driven by differences in length of the manubrium of the malleus. Morphological variation of extant hominid (gorilla, chimpanzee, and human) ossicles was studied in detail with a large sample by Quam et al. (2014). The lever ratio was found to be close (gorilla) or equal (chimpanzee) to the mean lever ratio found for haplorhines by Coleman and Ross (2004), whereas in humans the lever ratio turned out to be clearly lower; in fact, humans have the lowest lever ratio among primates (for functional inferences of the hominid lever ratios, see Quam, Martínez, Rosa, and Arsuaga, Chap. 8).